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Mosquitoes from Eight Geographical Locations of Sri Lanka Thilini C

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Mosquitoes from Eight Geographical Locations of Sri Lanka Thilini C Weeraratne et al. Malar J (2017) 16:234 DOI 10.1186/s12936-017-1876-y Malaria Journal RESEARCH Open Access Molecular characterization of Anopheline (Diptera: Culicidae) mosquitoes from eight geographical locations of Sri Lanka Thilini C. Weeraratne1, Sinnathambi N. Surendran2, Lisa J. Reimer3, Charles S. Wondji3, M. Devika B. Perera4, Catherine Walton5 and S. H. P. Parakrama Karunaratne1,6* Abstract Background: Genus Anopheles is a major mosquito group of interest in Sri Lanka as it includes vectors of malaria and its members exist as species complexes. Taxonomy of the group is mainly based on morphological features, which are not conclusive and can be easily erased while handling the specimens. A combined efort, using morphology and DNA barcoding (using the markers cytochrome c oxidase subunit I (COI) gene and internal transcribed spacer 2 (ITS2) region, was made during the present study to recognize anophelines collected from eight districts of Sri Lanka for the frst time. Methods: Cytochrome c oxidase subunit I and ITS2 regions of morphologically identifed anopheline mosquitoes from Sri Lanka were sequenced. These sequences together with GenBank sequences were used in phylogenetic tree construction and molecular characterization of mosquitoes. Results: According to morphological identifcation, the feld-collected adult mosquitoes belonged to 15 species, i.e., Anopheles aconitus, Anopheles annularis, Anopheles barbirostris, Anopheles culicifacies, Anopheles jamesii, Anopheles karwari, Anopheles maculatus, Anopheles nigerrimus, Anopheles pallidus, Anopheles peditaeniatus, Anopheles pseudo- jamesi, Anopheles subpictus, Anopheles tessellatus, Anopheles vagus, and Anopheles varuna. However, analysis of 123 COI sequences (445 bp) (16 clades supported by strong bootstrap value in the neighbour joining tree and inter-specifc distances of >3%) showed that there are 16 distinct species. Identity of the morphologically identifed species, except An. subpictus, was comparable with the DNA barcoding results. COI sequence analysis showed that morphologically identifed An. subpictus is composed of two genetic entities: An. subpictus species A and species B (inter-specifc K2P distance 0.128). All the four haplotypes of An. culicifacies discovered during the present study belonged to a single species. ITS2 sequences (542 bp) were obtained for all the species except for An. barbirostris, An. subpictus species B, An. tessellatus, and An. varuna. Each of these sequences was represented by a single species-specifc haplotype. Conclusions: The present study refects the importance and feasibility of COI and ITS2 genetic markers in identifying anophelines and their sibling species, and the signifcance of integrated systematic approach in mosquito taxonomy. Wide distribution of malaria vectors in the country perhaps indicates the potential for re-emergence of malaria in the country. Keywords: Anopheles, DNA barcoding, COI, ITS2, Mosquitoes, Taxonomy, Sri Lanka *Correspondence: [email protected]; [email protected] 1 Department of Zoology, Faculty of Science, University of Peradeniya, Peradeniya, Sri Lanka Full list of author information is available at the end of the article © The Author(s) 2017. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Weeraratne et al. Malar J (2017) 16:234 Page 2 of 14 Background Anopheles culicifacies and Anopheles subpictus exist as Species identifcation is essential for many biological species complexes [18–20]. Among the two An. culicifa- studies. Morphological characters and DNA barcoding cies species B and E found in Sri Lanka, species E is the are two major approaches used in species identifcation. primary vector of malaria in the country [18]. Anoph- Te modern system of taxonomy, referred to as ‘DNA eles subpictus (four sibling species viz. A, B, C and D) is barcoding’, which is based on molecular techniques, has considered the major vector of malaria in Jafna district become increasingly popular as it potentially produces and the secondary vector in other parts of the country results with very high precision and accuracy within a [21]. Several studies have found higher malaria sporo- short period of time, compared to traditional morphol- zite rates in An. subpictus than An. culicifacies during the ogy-based taxonomy. DNA barcoding is currently used peak transmission period in Jafna district [22, 23]. Fur- as a guide in biodiversity conservation and management ther, Anopheles aconitus, Anopheles annularis, Anopheles programmes due to its ability to confrm the identity of barbirostris, Anopheles nigerrimus, Anopheles pallidus, organisms, to infer the presence of new/endangered/ Anopheles peditaeniatus, Anopheles tessellatus, Anophe- invasive/cryptic species and to estimate genetic diversity les vagus, and Anopheles varuna are considered potential among individuals of a species [1]. vectors of malaria [24, 25]. Due to their importance in disease transmission, mos- In Sri Lanka, mosquito identifcation has mainly relied quitoes are one of the most intensely barcoded group of on taxonomic keys based on external morphological fea- insects, although many species are still to be identifed tures of adult and larval stages. However, a few studies and barcoded [2]. Further, mosquito species may exist as have attempted to use DNA barcodes to describe a few species complexes and sibling species of a given complex species, i.e., An. culicifacies [26, 27], An. subpictus [18], often show diferent feeding behaviour, biting habits, vec- An. barbirostris [28], and Anopheles sundaicus [29], from tor competence, distribution, and thereby diferent vec- limited geographic locations. Te country urgently needs torial capacities. Accurate and precise identifcation of a well planned molecular and morphology-based tax- mosquito species and sibling species is vital in planning onomy to characterize its anopheline population. Te vector control strategies. Since these sibling species can- present study aims to provide both morphological and not be distinguished by external morphological features, molecular taxonomic (DNA barcoding) information molecular taxonomy is required to obtain reliable infor- about Anopheles mosquitoes collected from diferent mation about the vector. geographical areas of Sri Lanka. Te importance of spe- Te most commonly used molecular markers/bar- cies identifcation using two molecular markers COI and code regions for mosquito barcoding studies are the ITS2 is also discussed. cytochrome c oxidase subunit I (COI) gene located in the mitochondrial genome (mtDNA) followed by the Methods internal transcribed spacer 2 (ITS2), a region from the Study sites nuclear ribosomal DNA. Several workers have used COI Mosquitoes were collected from eight study sites as the only marker in mosquito species recognition and located in eight districts in Sri Lanka: Kalmunai in in investigating their molecular evolution [3–9]. How- Ampara district, Haldummulla in Badulla district, Bat- ever, some studies have shown that mosquito identifca- ticaloa in Batticaloa district, Tirunelveli in Jafna dis- tion through COI alone is not always sufcient to make trict, Wariyapola in Kurunegala district, Matale in precise conclusions and the need for genetic examina- Matale district, Kattai-Adampan in Mannar district, tion using analysis of faster evolving regions, such as and Adikarigama in Nuwara-Eliya district (Fig. 1). Tese ITS2, has been emphasized [8]. ITS2 regions alone have sites are located in fve diferent climatic zones, i.e., been used in distinguishing closely related mosquito spe- Adikarigama in up-country wet zone (>900 m eleva- cies belonging to various genera such as Anopheles [10], tion, >2500 mm rainfall); Matale in mid-country wet Culex [11] and Aedes [12]. Moreover, it has been indi- zone (300–900 m elevation, >2500 mm rainfall); Hal- cated that more reliable information about species could dummulla in up-country intermediate zone (>900 m be obtained if several molecular markers are used simul- elevation, 1750–2500 mm rainfall); Wariyapola in low- taneously [13, 14]. country intermediate zone (0–300 m elevation, 1750– Te mosquito fauna in Sri Lanka comprises 141 spe- 2500 mm rainfall); Kalmunai, Batticaloa, Tirunelveli, cies belonging to 17 genera [15–17]. Out of these, 16.31% Katti-Adampan in low-country dry zone (0–300 m ele- (23 species) are anophelines. An accurate and detailed vation, <1750 mm rainfall, with a distinct dry period) species characterization of members of this genus is (Fig. 1). Habitat types of each study site are presented in required. In Sri Lanka, major malaria vector species Additional fle 1. Weeraratne et al. Malar J (2017) 16:234 Page 3 of 14 Fig. 1 Map of Sri Lanka showing the districts and the collection sites (1–8) from which mosquitoes were collected for the DNA barcoding study (elevations are given in parentheses) Mosquito collection morphological and molecular identifcations. Morpho- Adult mosquitoes were collected using cattle-baited traps logical identifcations to species or complex
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